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IntroductionCochlear implants (CIs) are the treatment of choice for severe to profound hearing loss. Variability in CI outcomes remains despite advances in technology and is attributed in part to differences in cortical processing. Studying these differences in CI users is technically challenging. Spectrally degraded stimuli presented to normal-hearing individuals approximate input to the central auditory system in CI users. This study used intracranial electroencephalography (iEEG) to investigate cortical processing of spectrally degraded speech.MethodsParticipants were adult neurosurgical epilepsy patients. Stimuli were utterances /aba/ and /ada/, spectrally degraded using a noise vocoder (1–4 bands) or presented without vocoding. The stimuli were presented in a two-alternative forced choice task. Cortical activity was recorded using depth and subdural iEEG electrodes. Electrode coverage included auditory core in posteromedial Heschl’s gyrus (HGPM), superior temporal gyrus (STG), ventral and dorsal auditory-related areas, and prefrontal and sensorimotor cortex. Analysis focused on high gamma (70–150 Hz) power augmentation and alpha (8–14 Hz) suppression.ResultsChance task performance occurred with 1–2 spectral bands and was near-ceiling for clear stimuli. Performance was variable with 3–4 bands, permitting identification of good and poor performers. There was no relationship between task performance and participants demographic, audiometric, neuropsychological, or clinical profiles. Several response patterns were identified based on magnitude and differences between stimulus conditions. HGPM responded strongly to all stimuli. A preference for clear speech emerged within non-core auditory cortex. Good performers typically had strong responses to all stimuli along the dorsal stream, including posterior STG, supramarginal, and precentral gyrus; a minority of sites in STG and supramarginal gyrus had a preference for vocoded stimuli. In poor performers, responses were typically restricted to clear speech. Alpha suppression was more pronounced in good performers. In contrast, poor performers exhibited a greater involvement of posterior middle temporal gyrus when listening to clear speech.DiscussionResponses to noise-vocoded speech provide insights into potential factors underlying CI outcome variability. The results emphasize differences in the balance of neural processing along the dorsal and ventral stream between good and poor performers, identify specific cortical regions that may have diagnostic and prognostic utility, and suggest potential targets for neuromodulation-based CI rehabilitation strategies.

In everyday life, predictable sensory stimuli are generally not ecologically informative. By contrast, novel or unexpected stimuli signal ecologically salient changes in the environment. This idea forms the basis of the predictive coding hypothesis: efficient sensory encoding minimizes neural activity associated with predictable backgrounds and emphasizes detection of changes in the environment. In real life, the brain must resolve multiple unexpected sensory events occurring over different time scales. The local/global deviant experimental paradigm examines auditory predictive coding over multiple time scales. For short-term novelty [hundreds of milliseconds; local deviance (LD)], sequences of identical sounds (/xxxxx/) are interspersed with sequences that contain deviants (/xxxxy/). Long-term novelty [several seconds; global deviance (GD)] is created using either (a) frequent /xxxxx/ and infrequent /xxxxy/ sequences, or (b) frequent /xxxxy/ and infrequent /xxxxx/ sequences. In scenario (a), there is both an LD and a GD effect (LDGD, “double surprise”). In (b), the global deviant is a local standard, i.e., sequence of identical sounds (LSGD). Cortical responses reflecting LD and GD originate in different brain areas, have a different time course, and are differentially sensitive to general anesthesia. Neural processes underlying LD and GD have been shown to interact, reflecting overlapping networks subserving the detection of novel auditory stimuli. This study examined these interactions using intracranial electroencephalography in neurosurgical patients. Subjects performed a GD target detection task before and during induction of anesthesia with propofol. Recordings were made from the auditory cortex, surrounding auditory-related and prefrontal cortex in awake, sedated, and unresponsive states. High gamma activity was used to measure the neural basis of local-by-global novelty interactions. Positive interaction was defined as a greater response to the double surprise LDGD condition compared to LSGD. Negative interaction was defined as a weaker response to LDGD. Positive interaction was more frequent than negative interaction and was primarily found in auditory cortex. Negative interaction typically occurred in prefrontal cortex and was more sensitive to general anesthesia. Temporo-parietal auditory-related areas exhibited both types of interaction. These interactions may have relevance in a clinical setting as biomarkers of conscious perception in the assessment of depth of anesthesia and disorders of consciousness.

Speech perception requires that sounds be transformed into speech-related objects with lexical and semantic meaning. It is unclear at what level in the auditory pathways this transformation emerges. Primary auditory cortex has been implicated in both representation of acoustic sound attributes and sound objects. While non-primary auditory cortex located on the posterolateral superior temporal gyrus (PLST) is clearly involved in acoustic-to-phonetic prelexical representations, it is unclear what role this region plays in auditory object formation. Additional data support the importance of prefrontal cortex in the formation of auditory objects, while other data would implicate this region in auditory object selection. To help clarify the respective roles of auditory and auditory-related cortex in the formation and selection of auditory objects, we examined high gamma activity simultaneously recorded directly from Heschl’s gyrus (HG), PLST and prefrontal cortex, while subjects performed auditory semantic detection tasks. Subjects were patients undergoing evaluation for treatment of medically intractable epilepsy. We found that activity in posteromedial HG and early activity on PLST was robust to sound stimuli regardless of their context, and minimally modulated by tasks. Later activity on PLST could be strongly modulated by semantic context, but not by behavioral performance. Activity within prefrontal cortex also was related to semantic context, and did co-vary with behavior. We propose that activity in posteromedial HG and early activity on PLST primarily reflect the representation of spectrotemporal sound attributes. Later activity on PLST represents a prelexical processing stage and is an intermediate step in the formation of word objects. Activity in prefrontal cortex appears directly involved in word object selection. The roles of other auditory and auditory-related cortical areas in the formation of word objects remain to be explored.